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(Stroke. 1995;26:930-936.)
© 1995 American Heart Association, Inc.
Articles |
Incidence and Causes of Strokes Associated With Pregnancy and Puerperium
A Study in Public Hospitals of Ile de France
From the Service de Neurologie, Hôpital Sainte Anne, and the Université René Descartes, Paris, France.
Correspondence to Prof J.-L. Mas, Service de Neurologie, Hôpital Sainte Anne, 1 rue Cabanis, 75674 Paris Cedex 14, France.
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose The incidence, causes, and prognosis of nonhemorrhagic strokes and intraparenchymal hemorrhages occurring in association with pregnancy or puerperium are poorly understood.
Methods We carried out a retrospective (1989 through 1991) and prospective (1992) study in 63 public maternities (348 295 deliveries) of the region of Ile de France (10 660 554 inhabitants) and in the neurology, neurosurgery, and intensive care units of the same geographic area. Records of women who suffered a cerebrovascular event during pregnancy or the first 2 weeks postpartum were reviewed by two study neurologists. Stroke was defined according to the criteria of the World Health Organization.
Results Thirty-one cases of strokes were identified, including 15 nonhemorrhagic strokes (including strokelike deficits associated with eclampsia) and 16 intraparenchymal hemorrhages, assessed in all cases by CT scan and/or MRI. The incidence of nonhemorrhagic strokes in women who delivered in public maternities of Ile de France was 4.3 per 100 000 deliveries (95% confidence interval, 2.4 to 7.1) and that of intraparenchymal hemorrhage was 4.6 per 100 000 deliveries (95% confidence interval, 2.6 to 7.5). Eclampsia accounted for 47% of cases of nonhemorrhagic strokes. The other causes were extracranial vertebral artery dissection, postpartum cerebral angiopathy, inherited protein S deficiency, and disseminated intravascular coagulation associated with amniotic fluid embolism. The cause remained undetermined in four cases despite extensive investigations. Eclampsia accounted for 44% of intraparenchymal hemorrhages. Another 37% were due to rupture of a vascular malformation. The cause remained undetermined in three cases. There were four maternal deaths (all associated with intraparenchymal hemorrhage), three of them in eclamptic women. Fetal mortality and prematurity were associated with eclampsia.
Conclusions The incidence of nonhemorrhagic stroke does not seem to be much increased during pregnancy and early puerperium. In contrast to that in the nonpregnant state, the frequency of intraparenchymal hemorrhage in pregnancy appears to be similar to that of nonhemorrhagic strokes, suggesting that pregnancy may increase the risk of cerebral hemorrhage. Eclampsia is the main cause of both nonhemorrhagic stroke and intraparenchymal hemorrhage. Intraparenchymal hemorrhage associated with eclampsia carries a poor prognosis.
Key Words: eclampsia • hemorrhage • pregnancy • puerperium • stroke
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Several studies have been devoted to cerebral venous thrombosis1 2 3 and rupture of cerebral vascular malformations during pregnancy.4 5 6 7 By contrast, the incidence, causes, and prognosis of nonhemorrhagic stroke and intraparenchymal hemorrhage (IPH) complicating pregnancy or puerperium are poorly understood. Most previous studies1 2 3 4 5 8 9 10 11 12 13 14 were based on series of pregnancies at single-referral institutions, which certainly creates a selection bias; most studies were reported before CT scan became widely available. The aim of this study was to assess the incidence and causes of nonhemorrhagic strokes and IPHs occurring in association with pregnancy and early puerperium on the basis of a large number of pregnancies in a well-defined geographic area and using modern imaging techniques.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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This study was conducted in the region of Ile de France from January 1989 through December 1992. The region of Ile de France is located in midnorthern France and includes the city of Paris. Its total population was 10 660 554 inhabitants in 1990. At the end of 1991, we contacted the 65 public maternities of this region (47 general hospitals, 17 academic hospitals, and 1 military hospital) to retrospectively identify women who had had a cerebrovascular event in association with pregnancy or puerperium between January 1989 and December 1991 and to prospectively identify women with such events between January 1992 and December 1992. To check on cases that may have eluded identification, we also contacted the neurology (n=27), neurosurgery (n=11), and intensive care (n=91) departments of the same geographic area. Sixty-three of the 65 public maternities, all neurology and neurosurgery departments, and 89 of the 91 intensive care units participated in the study. According to the Direction Regionale des Affaires Sanitaires et Sociales, there were 669 680 deliveries in the whole Ile de France area during the study period, of which 348 295 (52%) were performed in the 63 public maternities.
We asked each center to identify from its record system all patients with a cerebrovascular event (of any type) occurring during pregnancy or puerperium. The medical records of these patients were reviewed by two study neurologists who selected cases of nonhemorrhagic stroke or IPH occurring in association with pregnancy or the first 2 weeks of puerperium. Stroke was defined as rapidly developing clinical symptoms and/or signs of focal, and at times global (applied to patients with intracranial hemorrhage in deep coma), loss of cerebral function with symptoms lasting more than 24 hours or leading to death, with no other apparent cause than vascular origin.15 Patients with cerebral venous thrombosis, transient ischemic attacks, and pure subarachnoid hemorrhages were excluded. We excluded cerebral venous thrombosis because it is a difficult entity to diagnose. Its clinical presentation is often misleading, and its diagnosis requires MRI (a technique not easily available in all centers during the study period) or angiography. In addition, cerebral venous thrombosis occurs much more frequently after the first week postpartum.
Risk factors of stroke before pregnancy (history of hypertension, diabetes mellitus, cigarette smoking, and hypercholesterolemia), neurological features (headaches, seizures, and impairment of consciousness, in addition to focal deficit), and obstetric data (parity, prenatal care, gestational age at onset of stroke, maternal outcome, outcome of previous pregnancies, mode of delivery, fetal death) were systematically recorded. Etiologic investigations of the stroke were reviewed. All patients had CT scan and/or MRI, 12-lead electrocardiography, standard blood and urine tests including coagulation profile (prothrombin and activated partial thromboplastin times, platelet count), and liver and renal function tests. Other investigations were performed in selected patients. The 15 patients with nonhemorrhagic stroke had the following investigations: cerebral angiography (n=10), ultrasonographic examination of cervical arteries (n=8), echocardiography (n=7, transesophageal in 3), antinuclear and antiphospholipid antibodies (n=8), and detailed coagulation studies (n=7). Of the 16 patients with IPH, 11 had cerebral angiography. The residual functional disability was assessed by the modified Rankin scale16 3 months to 1 year after the stroke.
Hypertension in pregnancy was defined according to the criteria of the International Federation of Obstetrics and Gynecology17 as one measurement of diastolic blood pressure >110 mm Hg or two consecutive measurements of diastolic blood pressure >90 mm Hg 4 or more hours apart. Preeclampsia was defined by hypertension in association with proteinuria, edema, and at times liver function and coagulation disturbances; eclampsia was defined as the development of seizures and/or coma in a preeclamptic woman in whom no other cause can be found; and the HELLP syndrome was defined by the association of hemolysis (H), elevated liver enzymes (EL), and low platelet count (LP).18 19
The frequency of stroke was derived from the number of strokes among women who delivered in the 63 public maternities of the region of Ile de France during 1989 through 1992, and the 95% confidence intervals (CIs) were computed.20 These rates were also expressed in incidence rates per 100 000 person-years of observation by multiplying the rates per 100 000 deliveries by 12:9. The difference in homogeneity between the annual number of strokes throughout the study period was assessed by means of the Poisson distribution.21
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Results |
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Thirty-nine strokes were identified during the 4-year period from 1989 through 1992. Eight patients were excluded from the study because the women delivered in private maternities (6 patients) or out of Ile de France (2 patients) and subsequently were referred to a public hospital. Five of these women had IPH (due to a ruptured arterial aneurysm or arteriovenous malformation in 2, eclampsia in 2, and acute pregnancy-induced hypertension in 1), and 3 had a nonhemorrhagic stroke (due to eclampsia in 1, peripartum cardiomyopathy in 1, and disseminated intravascular coagulation associated with obstetric hemorrhage in 1).
The thirty-one remaining women with stroke (15 nonhemorrhagic strokes and 16 IPHs) delivered in public maternities of Ile de France. About 85% of the cases were identified from the files of the public maternities; the remaining cases were identified from the neurology, neurosurgery, and intensive care departments. There were no statistically significant differences in the annual number of strokes throughout the study period. The incidence of nonhemorrhagic strokes (n=15, including strokelike deficits associated with eclampsia) in women who delivered in public maternities of Ile de France was 4.3 per 100 000 deliveries (95% CI, 2.4 to 7.1) or 5.7 per 100 000 person-years of observation (95% CI, 3.2 to 9.4), and the incidence of IPH (n=16) was 4.6 per 100 000 deliveries (95% CI, 2.6 to 7.5) or 6.1 per 100 000 person-years of observation (95% CI, 3.5 to 9.9).
Nonhemorrhagic Strokes (n=15)
The mean maternal age at the time of stroke was 30.2 years (range,
19 to 40 years). Thirteen women were white, 2 were black. Five women
were multiparous with a parity ranging from two to four. None of them
had a previous history of neurological disorder associated with
pregnancy. Among the 7 eclamptic women, 6 were nulliparous. All
patients except 2 had adequate prenatal care. Risk factors for stroke
included cigarette smoking in 3 patients (2 had quit the habit before
pregnancy). The gestational age at the time of stroke is shown in Fig 1
.
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The causes of nonhemorrhagic strokes are shown in Table 1. Toxemia (eclampsia in 6 cases, preeclampsia in 1)
accounted for 47% of cases; eclampsia was associated with a HELLP
syndrome in 4 cases. Early cerebral angiography was performed in 2
patients and showed no abnormalities. One woman presented with
typical postpartum cerebral angiopathy, with severe headache of sudden
onset, normal cerebrospinal fluid, and multiple segmental stenoses of
medium-sized cerebral arteries, which had cleared on control
angiography 3 months later; focal signs were not prominent. Another
woman had severe neck pain and a lateral medullary syndrome. The
diagnosis of extracranial vertebral artery dissection was confirmed by
angiography and cervical MRI. The case of amniotic fluid embolism was
diagnosed on cytological examination of pulmonary artery samples from a
Swan-Ganz catheter. In the woman with protein S deficiency, MRI showed
an infarct in the middle cerebral artery territory and excluded
thrombosis of a dural venous sinus. The cause of stroke remained
undetermined in 4 patients despite extensive investigations including
cerebral angiography, echocardiography (transesophageal in 2 with a
contrast study), immunologic (antinuclear and antiphospholipid
antibodies), and coagulation tests (protein S, protein C, and
antithrombin III).
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In addition to focal deficits, the clinical features included headache in 11 patients, seizures in 6, and impairment of consciousness in 5. None of the noneclamptic women had seizures. Among the 7 eclamptic women, CT showed cerebral edema in 2, bilateral and symmetrical focal hypodensities in occipital lobes (n=1) or centrum semiovale and internal capsules (n=2), and was normal in 2. One eclamptic woman had an early MRI showing multifocal areas of increased signal intensity on T2-weighted images in the hemispheric white matter. Except for 1 patient who had persistent lesions in the internal capsules, control neuroimaging studies performed a few weeks later were normal. Among the 8 noneclamptic women, CT scan showed a cerebral infarct in the middle cerebral artery territory in 5, in the superficial and deep posterior cerebral artery territory in 1, and a thalamic infarct in 1 and was normal in 1.
Cesarean section was performed in 6 patients because of fetal distress
(3 patients), maternal distress (3 patients), or obstetric
considerations (3 patients). There was no maternal death secondary to
stroke. Five women were left with mild to moderate residual
neurological deficit, with a modified Rankin score ranging from 1 (3
patients) to 2 (2 patients). One additional patient had residual
epilepsy. There were two stillbirths and four premature deliveries
(Table 3).
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Intraparenchymal Hemorrhage (n=16)
The mean maternal age at the time of hemorrhage was 31 years
(range, 23 to 50 years); 13 patients were white and 3 were black. Nine
women were multiparous with a parity ranging from two to six; none of
them had a previous history of neurological disorder associated with
pregnancy. Among the 7 eclamptic women, 3 were multiparous with a
parity ranging from five to six. Three women had no prenatal care. Risk
factors for stroke included chronic hypertension in 1 and a past
history of cigarette smoking in 2. The gestational age at the time of
bleeding according to the main etiologic subgroups is summarized in Fig 2.
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The causes of brain hemorrhages are shown in Table 2.
IPH was attributed to eclampsia in 7 cases (44%); eclampsia was
associated with a HELLP syndrome in 2 cases and with disseminated
intravascular coagulation in 2 cases. In 3 patients with eclampsia, a
vascular malformation was excluded by a cerebral angiography; another
woman had a delayed MRI that showed only the sequelae of the hematoma.
Three eclamptic women died before angiography could be performed;
autopsy in 1 patient did not reveal any alternative cause of
hemorrhage. A ruptured vascular malformation accounted for 37% of
cases. The diagnoses of the two arterial aneurysms and the two
arteriovenous malformations were confirmed by surgery and histology.
Both cavernous angiomas were suspected on MRI performed 3 and 4 months
after the bleeding and subsequently confirmed by histology. The cause
of bleeding remained undetermined in 3 patients; 2 had an extensive
etiologic workup including repeated cerebral angiographies, and 1 died
rapidly, before any investigation could be performed.
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In addition to focal deficits, the clinical features included headaches in 13 cases, seizures in 12, and impairment of consciousness in 13. Among the 9 noneclamptic women, 3 had hypertension and/or seizures. The location of the hemorrhage was lobar in 10 patients (eclampsia in 4), lenticular-capsular in 3 patients (eclampsia in 1), brain stem in 2 patients (eclampsia in 2), and cerebellar in 1 patient.
All patients with ruptured vascular malformation underwent neurosurgery
after delivery. In 4 patients emergency neurosurgery was performed
because of a threatening hematoma. Cesarean section was performed in 14
patients because of fetal distress (7 patients), maternal distress (9
patients), placenta previa (1 patient), a wish to expedite delivery (1
patient), or prevention of intracranial hypertension during labor (1
patient). Four women died: 3 had eclampsia, and 1 had IPH of
undetermined etiology. Among the surviving patients, 8 had mild to
moderate residual neurological deficit with a modified Rankin score
ranging from 1 (3 patients) to 3 (3 patients). There were two
stillbirths and seven premature deliveries (Table 3
).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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In contrast to most previous studies that identified strokes at single-referral maternity hospitals,1 2 3 4 5 8 9 10 11 12 13 14 our study was conducted in 63 public maternities in a well-defined geographic area. The study, however, is subject to potential criticisms. First, because it was hospital-based, the study could not have included patients for whom hospitalization was not requested or patients referred to hospital departments not involved in the study. However, it would be quite unusual for a pregnant (or early puerperial) woman residing in the region of Ile de France (which provides many specialized hospital facilities) not to be referred to her maternity or to one of the neurology, neurosurgery, or intensive care departments of the same geographic area in the event of a focal deficit lasting more than 24 hours. Second, the study was based on public maternities of Ile de France, which account for 52% of all deliveries performed in the whole region of Ile de France. As women with high-risk or complicated pregnancy are more likely to be followed up in or referred to public academic hospitals, an overestimation of stroke incidence is possible. To reduce this bias, we based our study on a large number of public maternities, the majority of which (75%) are not referral academic centers. Finally, as the identification of patients with cerebrovascular events was partly retrospective, some cases (particularly the less serious ones) may have been missed, leading to an underestimation of stroke incidence and an overrepresentation of more severe strokes, such as hemorrhagic ones. To improve the identification of cases, we also contacted the neurology, neurosurgery, and intensive care units of the same geographic area. These sources yielded 5 cases (16%) that had not been recorded in the files of public maternities. The lack of significant differences in the number of strokes identified each year suggests consistency in the retrospective and prospective identification of cases.
Nonhemorrhagic Strokes
The incidence rates for ischemic strokes associated with
pregnancy or puerperium vary in the literature from 5 to 210 per
100 000 deliveries.1 2 8 9 10 11 12 13 14 Considering a mean incidence
of approximately one cerebral infarction for 3000 pregnancies (44
cerebral infarctions per 100 000 years of pregnancy observation) in
previous studies and an incidence of 3.5 ischemic strokes per
100 000 population per year in Rochester, Minnesota, for women aged 15
through 35 years, Wiebers22 estimated that pregnancy
increases the likelihood of cerebral infarction to about 13 times the
rate expected outside of pregnancy. These figures, however, may not be
representative of the actual incidence of pregnancy-associated
ischemic strokes because most previous studies provide
estimates based on series of pregnancies at single-referral academic
institutions, which certainly creates a selection bias. Indeed, in our
study, pregnancy-related strokes were confined to only 20 of the 63
public maternities, including 11 maternities belonging to academic
hospitals. A further issue regarding previous incidence rates relates
to the mechanism of cerebral ischemia. Many studies were
reported before 1965, and in most of them cerebral ischemia was
thought to be due to cerebral venous thrombosis, although in most cases
the nature of the pathological lesion was assumed rather than
proved.
Two previous studies provide estimates of the incidence of arterial ischemic strokes associated with pregnancy or puerperium. Cross et al13 identified 31 cases of ischemic carotid territory stroke in pregnant or puerperial women in the neurosurgery unit at Killearn Hospital of Glasgow during the 10-year period of 1956 through 1967. On the presumption that most cases of major carotid strokes in pregnant women living in the western region of Scotland were referred to the neurosurgical unit, the authors suggested that the frequency of cerebral infarction was approximately 5 cases per 100 000 deliveries. Wiebers and Whisnant23 identified only one instance of cerebral infarction and no instance of IPH in pregnant women in the well-defined population of Rochester, Minnesota, from 1955 through 1979. During this time, there were 26 099 live births among residents of Rochester, giving an incidence rate of 3.8 cerebral infarctions per 100 000 deliveries (5.1 per 100 000 person-years of observation). Our incidence data (4.3 per 100 000 deliveries; 95% CI, 2.4 to 7.1) are very close to those found in these studies and do not seem to be much different from those for all women of childbearing age in occidental countries.23 24 25
Eclampsia accounted for 47% of nonhemorrhagic strokes in our study. In addition to headaches, seizures, and/or altered consciousness, all patients had focal deficits of sudden onset consistent with a clinical diagnosis of stroke.15 Except for one patient who had a persistent neurological deficit and bilateral brain infarction on neuroimaging, the other patients had focal deficits that resolved in a matter of days. In these cases, neuroimaging studies were normal or showed bilateral and symmetrical cortical and/or subcortical abnormalities, most prominently in the posterior areas, which matched previous descriptions of CT and MRI in patients with severe preeclampsia or eclampsia.26 27 28 The CT and MRI changes were no longer present on the control neuroimaging studies performed a few weeks later. The precise pathogenesis of these short-lasting focal deficits, as well as of other central nervous system changes associated with eclampsia, remains poorly understood.19 In addition to cerebral hemorrhages, autopsy studies29 30 31 of women dying from eclampsia have shown varying degrees of cerebral edema, cortical and white matter microinfarcts, and a vasculopathy involving arterioles and capillaries. These findings, however, may not be representative of surviving patients. The reversibility of the neurological clinical signs and neuroradiological lesions in most cases argues against the existence of true cerebral ischemic necrosis. The clinical and neuroimaging findings are more consistent with local edema, which is thought to result from the vasomotor disturbances of hypertension.31
The other pregnancy-specific causes of nonhemorrhagic stroke are much rarer and include amniotic embolism31 and choriocarcinoma.32 It is unclear whether peripartum cardiomyopathy33 is a pregnancy-specific disorder or merely unmasked by gestational physiological stresses. Postpartum cerebral angiopathy is a reversible clinicoradiological syndrome that develops shortly after a normal pregnancy.34 A similar syndrome has been reported outside of pregnancy under various nosologies.35 Besides the causes that are peculiar to pregnancy, any of the known causes of stroke in the young may also occur during pregnancy,36 and the etiologic evaluation should proceed as in the nonpregnant state. Carotid and vertebral dissection is recognized as a cause of stroke in the young with increasing frequency, and dissection has been described in association with pregnancy or puerperium.37 About a fourth of all cerebral infarctions during pregnancy have been related to atherosclerosis,22 but this was based only on angiographic evidence of occlusion of the internal or middle cerebral artery,1 38 without verified atherosclerotic lesions in most cases. No case in our series was attributed to atherosclerosis. Finally, the cause of the ischemic stroke may remain undetermined despite extensive investigations (four cases in our study). Whether coagulation39 and vessel wall40 changes associated with pregnancy play a role in the occurrence of these otherwise unexplained ischemic strokes is unknown.
Intraparenchymal Hemorrhages
Data specifically devoted to the incidence of IPH are very scanty.
In the obstetric population at Parkland Memorial Hospital (Dallas,
Texas),14 four patients with IPH were identified among
nearly 90 000 women delivering during the 6.5-year period from 1984
through mid-1990 (4.4 per 100 000 deliveries). In studies devoted to
stroke incidence in young women, ischemic strokes have usually
been found to be much more frequent than IPHs.24 25 41 Our
finding that in pregnancy IPH (4.6 per 100 000 deliveries) was as
common as ischemic stroke (4.3 per 100 000 deliveries)
suggests that pregnancy may increase the risk of cerebral
hemorrhage.
Eclampsia accounted for 44% of IPHs in the present study (Table 2). IPH is a common finding in women dying from eclampsia, and it is
generally agreed that hemorrhage is a result of severe
hypertension,30 31 although coagulation disorders
associated with eclampsia19 may also play a role. A
ruptured vascular malformation was the second cause (37%) of IPH in
our study (Table 2). In two cases, cerebral hemorrhage was due to
rupture of a cavernous angioma, which to our knowledge has not been
previously reported in pregnancy. Whether and to what extent
hemodynamic and other physiological changes of pregnancy and
delivery42 increase the risk of bleeding from a vascular
malformation during gestation remain unsettled.6 7 In the
present study, no woman with a ruptured vascular malformation bled
during labor or delivery, and four women had one or two previous
successful pregnancies and vaginal deliveries without
complications.
The prognosis of IPH was more severe than that of nonhemorrhagic stroke
(Table 3), with four deaths, three of them in eclamptic women. Three of
the 7 women with eclampsia-associated IPH died, and 4 had neurological
sequelae compared with no death and only one persistent neurological
deficit in the 7 women with eclampsia-associated nonhemorrhagic stroke.
These findings confirm the poor maternal prognosis associated with
eclampsia complicated by brain hemorrhage. As with ischemic
strokes, fetal mortality and prematurity were associated with eclampsia
(Table 3).
In conclusion, this study provides estimates of the incidence of nonhemorrhagic strokes and IPHs during pregnancy and early puerperium based on a large number of pregnancies in a well-defined geographic area. The incidence of nonhemorrhagic strokes does not seem to be much increased during pregnancy and early puerperium. In contrast to the nonpregnant state, the frequency of IPHs appears to be similar to that of nonhemorrhagic strokes, suggesting that pregnancy may increase the risk of cerebral hemorrhage. The study highlights the importance of eclampsia as a cause of both nonhemorrhagic and hemorrhagic strokes.
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Acknowledgments |
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We thank Prof C. Tchobrousky for her invaluable help in the analysis of obstetric data and Dr C. Tzourio for statistical advice.
Study Participants
Public Maternities
Argenteuil (A. Landais, M. Piquet); Arpajon (J. Sebaoun);
Aulnay-sous-Bois (M.C. Boulanger); Baudelocque, Paris (E. Papiernik);
Beaujon, Clichy (M. Levardon); Beaumont-sur-Oise (J. Vu); A.
Béclère, Clamart (D. Edouard, R. Friedman); Bégin,
Saint Mandé (G. Charles); Bichat, Paris (P. Madelanat);
Boucicaut, Paris (R. Taurelle); Corbeil (J. Gérard); Coulommiers
(M. Mailhac); Courbevoie (B. Parent); Créteil (J. Milliez, B.
Paniel); R. Debré, Paris (P. Blot); Dourdan (A. Guth); Evry (D.
Galli-Douani); Etampes (C. Raini); Foch, Suresnes (J.C. Colau);
Fontainebleau (M.C. Cosnefroy, A. Dupont, P.E. Lhuillier); Gonesse (B.
Dauptain); Hôpital des Diaconesses, Paris (D. Collard, A. Ioan);
Hôpital International de l'Université de Paris, Paris (F.
Challier, H. Cohen, C. Prevost-Saglier); Hôpital
Franco-Britannique, Levallois-Perret (J. Jansé Marec);
Hôpital des Metallurgistes, Paris (J.M. Cheynier, D. Lachaux);
Hôpital Nord 92, Villeneuve-la-Garenne (S. Bizieau);
Juvisy-sur-Orge (C. Ducomun, L. Weil); Lagny (G. Algava);
Lariboisière, Paris (N. Ciraru-Vigneron, J. Ravina); Les Lilas
(F. Laiter, G. Strouk); Longjumeau (R. Bronstein, B. Greffe);
Mantes-la-Jolie (J.C. Berardi); Meaux (R. Gauzit, F. Michel, B. Morel);
Melun (T. Kleitz, P. Theron); Meulan (B. Robichez);
Montereau-Fault-Yvonne (J.L. Lucas); Montfermeil (J.F. Ropert);
Montmorency (J. Morvan); Montreuil (P. Crimail); L. Mourier, Colombes
(P. Engelman); Nanterre (J.A. Cacault); Nemours (M. Bredon);
Neuilly-sur-Seine (J.N. Botto); Notre-Dame-de-Bon-Secours, Paris (S. de
Kermadec-Barrier); Orsay (F.X. Thorin);
Pitié-Salpétrière, Paris (Y. Darbois, J. Sebacher);
Poissy (D. Lewin, P. Rosenberg); Pontoise (H. Berseneff, J.M. Muray);
Port-Royal, Paris (M. Dommergues, C. Tchobroutsky); Provins (F.
Ruppli); Rambouillet (J.X. L'hoir); J. Rostand, Ivry-sur-Seine (D.
Pathier); Rothschild, Paris (A. Pigné); Saint-Antoine, Paris (J.
Barrat, J. Milliez); Saint-Denis (C. Bazin); Saint-Germain-en-Laye (F.
Clement, F. Barbier, K. Lobjoit); Saint-Maurice (R. Jeny);
Saint-Vincent-de-Paul, Paris (J. Chavinié); Sèvres (J.
Belaisch-Allart, J. Loffredo); Tenon, Paris (S. Uzan); J. Verdier,
Bondy (J. Santarelli); Versailles (P. Lasfargues);
Villeneuve-Saint-Georges (B. Maria).
Neurology Departments
Argenteuil (P. Davous); Aulnay-sous-Bois (Y. Lanoë);
Avicenne, Bobigny (P. Delaporte); Beaujon, Clichy (H. Dehen, F.
Lisowosky, M. Masson); Bicêtre, Kremlin-Bicêtre (G. Said);
Corbeil (A. Morel-Maroger); Créteil (C. Meyrignac); Foch,
Suresnes (J.L. Truelle); Fondation A. de Rothschild, Paris (A.
Bouchareine, F. Mikol); Lariboisière, Paris (M. Haguenau, F.
Woimant); H. Mondor, Créteil (J.D. Degos); Montereau-Fault-Yvonne
(J.F. Doubrère); Pitié-Salpétrière, Paris (Y.
Agid, P. Brunet, F. Chain, C. Derouesné, D. Laplane, O.
Lyon-Caen, G. Rancurel, M. Vidailhet); Pontoise (H. Duclos);
Sainte-Anne, Paris (C. Lamy, J.L. Mas, J. de Recondo); Saint-Antoine,
Paris (P. Amarenco, M.G. Bousser); Saint-Denis (T. de Broucker);
Saint-Germain-en-Laye (H. Cambon, A. Richer); Saint-Joseph, Paris (C.F.
Degos); Tenon, Paris (A. Guillard, E. Roullet); Val-de-Grâce,
Paris (D. Bequet).
Neurosurgery Departments
Beaujon, Clichy (I. Arnulf, A. Rey); H. Dunant, Paris (J.B.
Thiebaut); Foch, Suresnes (P. Derome); Fondation A. de Rothschild,
Paris (G. Robert, M. Sachs); Bicêtre, Kremlin-Bicêtre (P.
David, M. Hurth); Lariboisière, Paris (J. Cophignon); H. Mondor,
Créteil (Y. Keravel); Pitié-Salpétrière, Paris
(P. Cornu; D. Fohanno, J. Philippon); Sainte-Anne, Paris (J.P.
Chodkiewicz, F.X. Roux); Val-de-Grâce, Paris (P. Pernot).
Intensive Care Departments
Argenteuil (G. Bleichner); Arpajon (J. Kaminski-Piton);
Aulnay-sous-Bois (P. Fouet); Avicenne, Bobigny (M. Cupa); Beaujon,
Clichy (J. Marty); Beaumont-sur-Oise (F. Fataud); A.
Béclère, Clamart (D. Benhamou, D. Edouard, K. Samii); C.
Bernard, Paris (F. Vachon, M. Wolff); Bicêtre,
Kremlin-Bicêtre (P. Auzepy, C. Richard, K. Samii); Bichat, Paris
(C. Deffargues, J.M. Desmonts, C. Gibert, J.L. Trouillet); Bligny,
Briis-sous-Forges (P. Andrivet, V. Canh); Boucicaut, Paris (E. Guerot,
J. Larousse); Broussais, Paris (M.T. Cousin, M. Safar); Bry-sur-Marne
(J.F. Loriferne); Cochin, Paris (C. Conseiller, J.F. Dhainaut); Corbeil
(D. Caen, C. Legall); Coulommiers (A. Dennetière); Créteil
(A. Boutros, J.P. Laporte); R. Debré, Paris (C. Deffargues, Y.
Nivoche); H. Dunant, Paris (C. Goerens); Eaubonne (C. Sicot); Etampes
(J.C. Lorenzo); Evry (R. Boiteau, F. Chamieh); Foch, Suresnes (M.
Fischler, P. Loirat); Fondation des Champs de Courses, Maisons-Laffitte
(R. Kawatli); Fondation A. de Rothschild, Paris (F. Sardnal);
Fontainebleau (P. Bicharzon); Hôpital des Diaconesses, Paris (Y.
Ravaud, F. Thomas); Gonesse (F. Blin, T. Marsepoil); Hôpital
International de l'Université de Paris, Paris (B. Herman);
Hôpital Suisse de Paris, Issy-les-Moulineaux (J.M. Korach);
Laennec, Paris (G. Barrier, J.L. Diehl, P. Even, D. Safran); Lagny (Y.
Guittard, J.L. Le Bonhomme); Lariboisière, Paris (E. Echter, J.M.
Guérin, J.M. Segrestaa); Longjumeau (P. de Rohan-Chabot);
Mantes-la-Jolie (E. Barre, J.L. Bourdain); Meaux (A. Combes); Melun
(M.C. Porta); Meulan (A. Blanc, J. Longchal); H. Mondor, Créteil
(P. Duvaldestin, F. Lemaire); Montereau-Fault-Yvonne (P. Paschal);
Montfermeil (J.M. Coulaud); Montmorency (L. Bernard); Montreuil (D.
Kleinknecht, J.L. Pallot); L. Mourier, Colombes (F. Coste, A.C.
Leclerc, G. Parmentier); Nanterre (G. Bussière);
Neuilly-sur-Seine (M. Moulias); Orsay (D. Benichou); Nemours (J.L.
Saclier); A. Paré, Boulogne (M. Chauvin, P. Guesnon, F. Jardin,
A. Margairaz); Pitié-Salpétrière, Paris (P. Viars);
R. Poincaré, Garches (D. Fraysse, P. Gajdos, J. Pasteyer); Poissy
(F. Nouailhat, J.P. Terville); Pontoise (G. Dezeros, M. Pescio, G.
Trouillet); Provins (B. Just); Rambouillet (N. Fadel); J. Rostand,
Ivry-sur-Seine (P. Viars); Rothschild, Paris (J.H. Gaudy);
Rueil-Malmaison (H. Chevalier); Sainte-Anne, Paris (L. Meignan);
Saint-Antoine, Paris (P. Amstutz, A. Lienhart); Saint-Denis (F.
Fraisse, L. Wingtin); Saint-Germain-en-Laye (D. Bertrand);
Saint-Joseph, Paris (J. Carlet); Saint-Louis, Paris (B. Eurin, J.R. Le
Gall); Saint-Michel, Paris (G. Goursot); Sèvres (J.C. Crabol, M.
Viehl); Tenon, Paris (F. Clergue, P. Deligne); Val-de-Grâce,
Paris (J.P. Bonsignour); J. Verdier, Bondy (J.L. Pourriat); Versailles
(S. Grobuis, L. Guyot); Villeneuve-Saint-Georges (M. Bombart, M.
Guilbaud); F. Widal, Paris (C. Bismuth).
Received January 17, 1995; revision received March 14, 1995; accepted March 16, 1995.
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